journal article·2017-10

Gold nanoparticles induce cell death and suppress migration of melanoma cells

Po-Hsuan Lu, Hsin-Ju Li, Hsun-Hsien Chang, Nan-Lin Wu, Chi-Feng Hung

Journal of Nanoparticle Research· Volume 19· Issue 10
Publisher page

Abstract

Diverse nanoparticles have been widely applied in different fields, including industries and biomedical sciences. Recent developments in nanotechnology have broadened the potential applications of nanotechnology in clinical diagnosis and medical therapy of malignant and non-malignant diseases. Gold nanoparticles (AuNPs) have been reported to possess unique physico-chemical properties; they have been investigated in studies on tumor growth and metastasis. Here, we explored the possible pharmacological functions of AuNPs on the mouse melanoma cell line, B16F10. We demonstrated that AuNPs of sizes 1–3, 3–5, and 10–15 nm exerted dose-dependent cytotoxic effects after 72-h treatments. AuNPs (4 and 10 ppm) of 1–3 and 3–5 nm were more cytotoxic than those of 10–15 nm. However, AuNPs of 1–3 nm were more cytotoxic against benign HaCaT keratinocytes than those of 3–5 nm. Thus, 4 ppm of AuNPs of 3–5 nm was considered relatively safe and an ideal candidate for this study. Further investigations revealed that AuNPs could induce sub-G1 phase accumulation, cleavage of caspase-3 and poly-(ADP-ribose) polymerase, and activation of JNK/p38. The expression of pro-apoptotic protein, Bax, was also induced. Furthermore, platelet-derived growth factor BB-induced migration and motility of melanoma cells were reduced after pretreatment with AuNPs of 3–5 nm. Adhesion assay showed that AuNPs of 3–5 nm could significantly suppress the adhesion of melanoma cells to collagen. In summary, AuNPs of 3–5 nm might be potential anti-tumor agents, as they were selectively cytotoxic against and inhibited motility of melanoma cells.
Source: openaire · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Nanoparticles: synthesis and applications · Nanoparticle-Based Drug Delivery · Gold and Silver Nanoparticles Synthesis and Applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (48)

Show source-provided references
1. Ali D, Alarifi S, Alkahtani S, AlKahtane AA, Almalik A (2015) Cerium oxide nanoparticles induce oxidative stress and genotoxicity in human skin melanoma cells. Cell Biochem Biophys 71:1643–1651. https://doi.org/10.1007/s12013-014-0386-610.1007/s12013-014-0386-6 ↗
2. Ali MRK, Wu Y, Ghosh D, Do BH, Chen K, Dawson MR, Fang N, Sulchek TA, El-Sayed MA (2017) Nuclear membrane-targeted gold nanoparticles inhibit cancer cell migration and invasion. ACS Nano 11:3716–3726. https://doi.org/10.1021/acsnano.6b0834510.1021/acsnano.6b08345 ↗
3. Almeida JP, Lin AY, Langsner RJ, Eckels P, Foster AE, Drezek RA (2014) In vivo immune cell distribution of gold nanoparticles in naive and tumor bearing mice. Small 10:812–819. https://doi.org/10.1002/smll.20130199810.1002/smll.201301998 ↗
4. Arooj S, Nazir S, Nadhman A, Ahmad N, Muhammad B, Ahmad I, Mazhar K, Abbasi R (2015) Novel ZnO:Ag nanocomposites induce significant oxidative stress in human fibroblast malignant melanoma (Ht144) cells. Beilstein J Nanotechnol 6:570–582. https://doi.org/10.3762/bjnano.6.5910.3762/bjnano.6.59 ↗
5. Arvizo RR, Rana S, Miranda OR, Bhattacharya R, Rotello VM, Mukherjee P (2011) Mechanism of anti-angiogenic property of gold nanoparticles: role of nanoparticle size and surface charge. Nanomedicine 7:580–587. https://doi.org/10.1016/j.nano.2011.01.01110.1016/j.nano.2011.01.011 ↗
6. Arvizo RR, Saha S, Wang E, Robertson JD, Bhattacharya R, Mukherjee P (2013) Inhibition of tumor growth and metastasis by a self-therapeutic nanoparticle. Proc Natl Acad Sci U S A 110:6700–6705. https://doi.org/10.1073/pnas.121454711010.1073/pnas.1214547110 ↗
7. Bei D, Meng J, Youan BB (2010) Engineering nanomedicines for improved melanoma therapy: progress and promises. Nanomedicine (Lond) 5:1385–1399. https://doi.org/10.2217/nnm.10.11710.2217/nnm.10.117 ↗
8. Bhattacharya U, Halder B, Mukhopadhyay S, Giri AK (2009) Role of oxidation-triggered activation of JNK and p38 MAPK in black tea polyphenols induced apoptotic death of A375 cells. Cancer Sci 100:1971–1978. https://doi.org/10.1111/j.1349-7006.2009.01251.x10.1111/j.1349-7006.2009.01251.x ↗
9. Brys AK, Gowda R, Loriaux DB, Robertson GP, Mosca PJ (2016) Nanotechnology-based strategies for combating toxicity and resistance in melanoma therapy. Biotechnol Adv 34:565–577. https://doi.org/10.1016/j.biotechadv.2016.01.00410.1016/j.biotechadv.2016.01.004 ↗
10. Cancer Genome Atlas N (2015) Genomic classification of cutaneous melanoma. Cell 161:1681–1696. https://doi.org/10.1016/j.cell.2015.05.04410.1016/j.cell.2015.05.044 ↗
11. Chan CM, Chang HH, Wang VC, Huang CL, Hung CF (2013) Inhibitory effects of resveratrol on PDGF-BB-induced retinal pigment epithelial cell migration via PDGFRbeta, PI3K/Akt and MAPK pathways. PLoS One 8:e56819. https://doi.org/10.1371/journal.pone.005681910.1371/journal.pone.0056819 ↗
12. Chithrani BD, Ghazani AA, Chan WC (2006) Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett 6:662–66810.1021/nl052396o ↗
13. Dreaden EC, Mackey MA, Huang X, Kang B, El-Sayed MA (2011) Beating cancer in multiple ways using nanogold. Chem Soc Rev 40:3391–3404. https://doi.org/10.1039/c0cs00180e10.1039/c0cs00180e ↗
14. Flockhart RJ, Webster DE, Qu K, Mascarenhas N, Kovalski J, Kretz M, Khavari PA (2012) BRAFV600E remodels the melanocyte transcriptome and induces BANCR to regulate melanoma cell migration. Genome Res 22:1006–1014. https://doi.org/10.1101/gr.140061.11210.1101/gr.140061.112 ↗
15. Freese C, Uboldi C, Gibson MI, Unger RE, Weksler BB, Romero IA, Couraud PO, Kirkpatrick CJ (2012) Uptake and cytotoxicity of citrate-coated gold nanospheres: comparative studies on human endothelial and epithelial cells. Part Fibre Toxicol 9:23. https://doi.org/10.1186/1743-8977-1189-1123.10.1186/1743-8977-1189-1123. ↗
16. Gowda R, Jones NR, Banerjee S, Robertson GP (2013) Use of nanotechnology to develop multi-drug inhibitors for cancer therapy. J Nanomed Nanotechnol 4. https://doi.org/10.4172/2157-7439.100018410.4172/2157-7439.1000184 ↗
17. Gowda R, Kardos G, Sharma A, Singh S, Robertson GP (2017) Nanoparticle-based celecoxib and plumbagin for the synergistic treatment of melanoma. Mol Cancer Ther 16:440–452. https://doi.org/10.1158/1535-7163.mct-16-028510.1158/1535-7163.mct-16-0285 ↗
18. Gu C, Wu H, Ge G, Li X, Guo Z, Bian Z, Xu J, Lu H, Chen X, Yang D (2016) In vitro effects of hollow gold nanoshells on human aortic endothelial cells. Nanoscale Res Lett 11:397. https://doi.org/10.1186/s11671-016-1620-510.1186/s11671-016-1620-5 ↗
19. Guerry D, Synnestvedt M, Elder DE, Schultz D (1993) Lessons from tumor progression: the invasive radial growth phase of melanoma is common, incapable of metastasis, and indolent. J Invest Dermatol 100:S342–S345. https://doi.org/10.1038/jid.1993.6010.1038/jid.1993.60 ↗
20. Hassan M, Alaoui A, Feyen O, Mirmohammadsadegh A, Essmann F, Tannapfel A, Gulbins E, Schulze-Osthoff K, Hengge UR (2008) The BH3-only member Noxa causes apoptosis in melanoma cells by multiple pathways. Oncogene 27:4557–4568. https://doi.org/10.1038/onc.2008.9010.1038/onc.2008.90 ↗
21. Huang CH, Li HJ, NL W, Hsiao CY, Lin CN, Chang HH, Hung CF (2016) Photoprotective effects of cycloheterophyllin against UVA-induced damage and oxidative stress in human dermal fibroblasts. PLoS One 11:e0161767. https://doi.org/10.1371/journal.pone.016176710.1371/journal.pone.0161767 ↗
22. Jain A, Ranjan S, Dasgupta N, Ramalingam C (2016) Nanomaterials in food and agriculture: an overview on their safety concerns and regulatory issues. Crit Rev Food Sci Nutr:1–21. https://doi.org/10.1080/10408398.2016.116036310.1080/10408398.2016.1160363 ↗
23. Kuphal S, Bauer R, Bosserhoff AK (2005) Integrin signaling in malignant melanoma. Cancer Metastasis Rev 24:195–222. https://doi.org/10.1007/s10555-005-1572-110.1007/s10555-005-1572-1 ↗
24. Lai TH, Shieh JM, Tsou CJ, Wu WB (2015) Gold nanoparticles induce heme oxygenase-1 expression through Nrf2 activation and Bach1 export in human vascular endothelial cells. Int J Nanomedicine 10:5925–5939. https://doi.org/10.2147/IJN.S8851410.2147/IJN.S88514 ↗
25. Li S, Huang X, Zhang D, Huang Q, Pei G, Wang L, Jiang W, Hu Q, Tan R, Hua ZC (2013) Requirement of PEA3 for transcriptional activation of FAK gene in tumor metastasis. PLoS One 8:e79336. https://doi.org/10.1371/journal.pone.007933610.1371/journal.pone.0079336 ↗
26. Luna-Vargas MP, Chipuk JE (2016) Physiological and pharmacological control of BAK, BAX, and beyond. Trends Cell Biol 26:906–917. https://doi.org/10.1016/j.tcb.2016.07.00210.1016/j.tcb.2016.07.002 ↗
27. Medina TM, Lewis KD (2016) The evolution of combined molecular targeted therapies to advance the therapeutic efficacy in melanoma: a highlight of vemurafenib and cobimetinib. Onco Targets Ther 9:3739–3752. https://doi.org/10.2147/OTT.S8677410.2147/OTT.S86774 ↗
28. Mohana-Kumaran N, Hill DS, Allen JD, Haass NK (2014) Targeting the intrinsic apoptosis pathway as a strategy for melanoma therapy. Pigment Cell Melanoma Res 27:525–539. https://doi.org/10.1111/pcmr.1224210.1111/pcmr.12242 ↗
29. Moro N, Mauch C, Zigrino P (2014) Metalloproteinases in melanoma. Eur J Cell Biol 93:23–29. https://doi.org/10.1016/j.ejcb.2014.01.00210.1016/j.ejcb.2014.01.002 ↗
30. Munoz-Alonso MJ, Gonzalez-Santiago L, Zarich N, Martinez T, Alvarez E, Rojas JM, Munoz A (2008) Plitidepsin has a dual effect inhibiting cell cycle and inducing apoptosis via Rac1/c-Jun NH2-terminal kinase activation in human melanoma cells. J Pharmacol Exp Ther 324:1093–1101. https://doi.org/10.1124/jpet.107.13266210.1124/jpet.107.132662 ↗
31. Olszanski AJ (2014) Current and future roles of targeted therapy and immunotherapy in advanced melanoma. J Manag Care Spec Pharm 20:346–356. 10.18553/jmcp.2014.20.4.34610.18553/jmcp.2014.20.4.346 ↗
32. Pan Y, Neuss S, Leifert A, Fischler M, Wen F, Simon U, Schmid G, Brandau W, Jahnen-Dechent W (2007) Size-dependent cytotoxicity of gold nanoparticles. Small 3:1941–1949. https://doi.org/10.1002/smll.20070037810.1002/smll.200700378 ↗
33. Pandya P, Orgaz JL, Sanz-Moreno V (2017) Modes of invasion during tumour dissemination. Mol Oncol 11:5–27. https://doi.org/10.1002/1878-0261.1201910.1002/1878-0261.12019 ↗
34. Paul CD, Mistriotis P, Konstantopoulos K (2017) Cancer cell motility: lessons from migration in confined spaces. Nat Rev Cancer 17:131–140. https://doi.org/10.1038/nrc.2016.12310.1038/nrc.2016.123 ↗
35. Pernodet N, Fang X, Sun Y, Bakhtina A, Ramakrishnan A, Sokolov J, Ulman A, Rafailovich M (2006) Adverse effects of citrate/gold nanoparticles on human dermal fibroblasts. Small 2:766–77310.1002/smll.200500492 ↗
36. Reddig PJ, Juliano RL (2005) Clinging to life: cell to matrix adhesion and cell survival. Cancer Metastasis Rev 24:425–439. https://doi.org/10.1007/s10555-005-5134-310.1007/s10555-005-5134-3 ↗
37. Saha S, Xiong X, Chakraborty PK, Shameer K, Arvizo RR, Kudgus RA, Dwivedi SK, Hossen MN, Gillies EM, Robertson JD, Dudley JT, Urrutia RA, Postier RG, Bhattacharya R, Mukherjee P (2016) Gold nanoparticle reprograms pancreatic tumor microenvironment and inhibits tumor growth. ACS Nano 10:10636–10651. https://doi.org/10.1021/acsnano.6b0223110.1021/acsnano.6b02231 ↗
38. Shieh JM, Huang TF, Hung CF, Chou KH, Tsai YJ, WB W (2010) Activation of c-Jun N-terminal kinase is essential for mitochondrial membrane potential change and apoptosis induced by doxycycline in melanoma cells. Br J Pharmacol 160:1171–1184. https://doi.org/10.1111/j.1476-5381.2010.00746.x10.1111/j.1476-5381.2010.00746.x ↗
39. Siegel RL, Miller KD, Jemal A (2016) Cancer statistics, 2016. CA Cancer J Clin 66:7–30. https://doi.org/10.3322/caac.2133210.3322/caac.21332 ↗
40. Steeg PS (2016) Targeting metastasis. Nat Rev Cancer 16:201–218. https://doi.org/10.1038/nrc.2016.2510.1038/nrc.2016.25 ↗
41. Tang JQ, Hou XY, Yang CS, Li YX, Xin Y, Guo WW, Wei ZP, Liu YQ, Jiang G (2017) Recent developments in nanomedicine for melanoma treatment. Int J Cancer. https://doi.org/10.1002/ijc.3070810.1002/ijc.30708 ↗
42. Tsai YY, Huang YH, Chao YL, KY H, Chin LT, Chou SH, Hour AL, Yao YD, CS T, Liang YJ, Tsai CY, HY W, Tan SW, Chen HM (2011) Identification of the nanogold particle-induced endoplasmic reticulum stress by omic techniques and systems biology analysis. ACS Nano 5:9354–9369. https://doi.org/10.1021/nn202777510.1021/nn2027775 ↗
43. Vieira LF, Lins MP, Viana IM, Dos Santos JE, Smaniotto S, Reis MD (2017) Metallic nanoparticles reduce the migration of human fibroblasts in vitro. Nanoscale Res Lett 12:200. https://doi.org/10.1186/s11671-11017-11982-1167310.1186/s11671-11017-11982-11673 ↗
44. Wang R, Brattain MG (2007) The maximal size of protein to diffuse through the nuclear pore is larger than 60kDa. FEBS Lett 581:3164–3170. https://doi.org/10.1016/j.febslet.2007.05.08210.1016/j.febslet.2007.05.082 ↗
45. Wei XL, Mo ZH, Li B, Wei JM (2007) Disruption of HepG2 cell adhesion by gold nanoparticle and paclitaxel disclosed by in situ QCM measurement. Colloids Surf B Biointerfaces 59:100–104. https://doi.org/10.1016/j.colsurfb.2007.04.01610.1016/j.colsurfb.2007.04.016 ↗
46. Wu NL, Chiang YC, Huang CC, Fang JY, Chen DF, Hung CF (2010) Zeaxanthin inhibits PDGF-BB-induced migration in human dermal fibroblasts. Exp Dermatol 19:e173–e181. https://doi.org/10.1111/j.1600-0625.2009.01036.x10.1111/j.1600-0625.2009.01036.x ↗
47. Wu NL, Fang JY, Chen M, CJ W, Huang CC, Hung CF (2011) Chrysin protects epidermal keratinocytes from UVA- and UVB-induced damage. J Agric Food Chem 59:8391–8400. https://doi.org/10.1021/jf200931t10.1021/jf200931t ↗
48. Yen HJ, Hsu SH, Tsai CL (2009) Cytotoxicity and immunological response of gold and silver nanoparticles of different sizes. Small 5:1553–1561. https://doi.org/10.1002/smll.20090012610.1002/smll.200900126 ↗